Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

Voss, Robert S.; Fleck, David W.; Jansa, Sharon A. ON THE DIAGNOSTIC CHARACTERS, ECOGEOGRAPHIC DISTRIBUTION, AND PHYLOGENETIC RELATIONSHIPS OF emiliae (DIDELPHIMORPHIA: DIDELPHIDAE: THYLAMYINI) Mastozoología Neotropical, vol. 16, núm. 2, diciembre, 2009, pp. 433-443 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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ON THE DIAGNOSTIC CHARACTERS, ECOGEOGRAPHIC DISTRIBUTION, AND PHYLOGENETIC RELATIONSHIPS OF Gracilinanus emiliae (DIDELPHIMORPHIA: DIDELPHIDAE: THYLAMYINI)

Robert S. Voss1, David W. Fleck2, and Sharon A. Jansa3

1 Department of Mammalogy, American Museum of Natural History, New York, NY 10024, U.S.A. [Corresponding author: ]. 2 Department of Anthropology, American Museum of Natural History, New York, NY 10024, U.S.A. 3 Bell Museum of Natural History and Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108, U.S.A.

ABSTRACT: Gracilinanus emiliae is a of gracile mouse that is currently known from fewer than a dozen specimens. The material we examined exhibits a distinc- tive suite of external and craniodental characters that are unlike those of any other con- generic species. We review all published records for G. emiliae, several of which are based on misidentifications or lost material, and we report a new specimen from northeast- ern Peru, the first to be recorded from that country, and the first to be unequivocally associated with primary lowland rain forest. The available distributional data suggest that G. emiliae (or a complex of cryptic taxa with the same morphological characters) is very widely distributed in Amazonia and perhaps also in Venezuelan coastal rain forests. Phy- logenetic analyses of morphological and molecular data suggest that G. emiliae is the sister taxon to other analyzed species of Gracilinanus, the biogeographic history of which is likely to be complex.

RESUMEN: Sobre los caracteres diagnósticos, distribución ecogeográfica y relaciones filogenéticas de Gracilinanus emiliae (Didelphimorphia: Didelphidae: Thylamyini). Gracilinanus emiliae es una especie de conocida a partir de menos de una docena de especímenes. El material examinado presenta rasgos externos y craniodentales distintivos, que difieren de los correspondientes a las restantes especies congenéricas. Revisamos todos los registros publicados de G. emiliae, algunos de los cuales son basados en identificaciones erróneas o material actualmente perdido, y reportamos un nuevo espécimen del noroeste de Perú, el primero registrado para este país, y el primero asociado inequívocamente con bosque húmedo primario de tierra baja. Los datos geográficos disponibles sugieren que G. emiliae (o un complejo de especies crípticas) tiene una distribución muy amplia en Amazonía y quizás también en los bosques húmedos de la costa de Venezuela. Los análisis filogenéticos de caracteres morfológicos y moleculares sugieren que G. emiliae es el grupo hermano de las restantes especies de Gracilinanus. La historia biogeográfica de este género es probablamente compleja.

Key words. Amazonia. . Marsupial. Neotropical. Rainforest.

Palabras claves. Amazonía. Mamífero. Marsupial. Neotropical. Selva.

Recibido 06 noviembre 2008. Aceptado 02 febrero 2009. Editor asociado: G D’Elía 434 Mastozoología Neotropical, 16(2):433-443, Mendoza, 2009 RS Voss et al. http://www.sarem.org.ar

INTRODUCTION is notably divergent from other congeneric species in several morphological traits (Voss Gracilianus emiliae was originally described et al., 2001, 2005). Although the monophyly by Thomas (1909) as a species of the didelphid of Gracilinanus was weakly supported in one marsupial . Thomas’s material recent analysis of sequence data from the consisted of a single specimen collected by nuclear IRBP gene (Voss et al., 2005), subse- Dr. Emilia Snethlage near Belém in the north- quent analyses incorporating sequence data eastern Brazilian state of Pará, and no addi- from the nuclear DMP1 locus (Jansa and Voss, tional material was reported by Tate (1933) 2005; Jansa et al., 2006) suggested that emiliae when he classified emiliae as a member of the may be more closely related to “Microtarsus Group” of Marmosa in his mono- than to other species of Gracilinanus. In ad- graphic revision of the genus. Cabrera (1958) dition to being a biogeographic outlier, emiliae subsequently assigned emiliae (along with thus appears to be evolutionarily divergent as many other species in Tate’s Microtarsus well. Group) to the subgenus , but Kirsch This paper reviews the diagnostic charac- and Calaby (1977) transferred it without com- ters of Gracilinanus emiliae, evaluates ment to the subgenus Marmosa. Gardner and ecogeographic information associated with Creighton (1989) placed emiliae in their new examined specimens, and reports a new speci- genus Gracilinanus, where it has remained to men from Peru that provides unambiguous date (Hershkovitz, 1992; Gardner, 2005; Voss evidence of habitat association. We also re- et al., 2005; Creighton and Gardner, 2008). port parsimony analyses of sequence data from Gracilinanus emiliae is biogeographically five nuclear loci that definitively resolve the unusual because it is one of only two species relationships of G. emiliae to other sequenced of Gracilinanus that have been reported from species of Gracilinanus and Cryptonanus. Amazonian lowland rainforests. Although a Together, these results substantially clarify the few specimens resembling G. agilis have been biogeographic and evolutionary significance of reported from lowland Amazonian rainforest this elusive and interesting marsupial. in SE Peru (e.g., by Solari et al., 2006), most species of Gracilinanus occur in other biomes, MATERIALS AND METHODS including montane forest (in the Andes and the Venezuelan coastal cordilleras), Atlantic The morphological specimens we examined and rain forest (in eastern , northeastern others mentioned below are preserved in the fol- Argentina, and eastern Paraguay), and the lowing collections (listed in order of their standard Cerrado (see maps in Hershkovitz, 1992 [fig. institutional abbreviations): AMNH, American Museum of Natural History (New York); BMNH, 1]; Brown, 2004 [figs. 16–23]). Unfortunately, Natural History Museum (London); FMNH, Field some Amazonian records of G. emiliae are Museum (Chicago); MNRJ, Museu Nacional (Rio based on misidentifications (Voss et al., 2001), de Janeiro); MUSM, Museo de Historia Natural, and it has therefore been suggested that the Universidad Nacional Mayor de San Marcos genus is absent from the central part of the (Lima); ROM, Royal Ontario Museum (Toronto); Amazon Basin (Costa et al., 2003; Patton and and USNM, National Museum of Natural History Costa, 2003). Because most records of G. (Washington, D.C.). emiliae that can be confirmed on the basis of We transcribed total length (nose to fleshy tail- examined specimens (mapped by Voss et al., tip, TL) and length of tail (basal flexure to fleshy tip, LT) from the labels of specimens obtained by 2001: fig. 10) are from localities adjacent to American collectors (who use the field measure- savanna landscapes, it is possible that this ment protocol described by Hall, 1981), and we species only occurs along the rainforest edge computed head-and-body length (HBL) by subtract- and not in mature, closed-canopy habitats. ing LT from TL. Alternatively, we transcribed head- A second problem concerns the phylogenetic and-body length and tail length directly from the relationships of Gracilinanus emiliae, which labels of specimens obtained by British collectors SYSTEMATICS OF Gracilinanus emiliae 435

(who follow a different field measurement proto- opposed to hairs that are basally gray and distally col). We also transcribed length of hind foot (heel white, cream, or buffy. to tip of longest claw, HF), length of ear (from The phylogenetic data we analyzed include 129 notch, Ear), and weight from specimen labels or characters that were scored from morphological field notes, but we sometimes remeasured HF on comparisons of skins, skulls, and fluid-preserved fluid-preserved specimens to check the accuracy material representing 43 didelphid species in 17 of values recorded by the collector, and we used genera. In order to root our analyses, we also scored our values whenever large discrepancies were character data from seven species of nondidelphid found. All external measurements are reported to that served as outgroups in our analy- the nearest millimeter (mm), and all weights are ses: one microbiotheriid (Dromiciops gliroides), reported to the nearest gram (g). two caenolestids (Caenolestes fuliginosus, Craniodental measurements were taken with digi- Rhyncholestes raphanurus), two dasyurids tal calipers and recorded to the nearest 0.01 mm, (Murexia longicaudatus, Sminthopsis but values reported herein are rounded to the near- crassicaudata), and two peramelids (Echymipera est 0.1 mm. The following dimensions were re- kalubu, Perameles gunni). The nonmolecular char- corded as illustrated by Voss et al. (2004: fig. 2): acters that we scored for these 50 terminal taxa Condylo-Basal Length (CBL), measured from the (defined by Voss and Jansa, 2009: appendix 3) occipital condyles to the anteriormost point of the include 39 from the integument (rhinarium, pel- premaxillae; Nasal Breadth (NB), measured be- age, manus, pes, mammae, pouch, cloaca, tail, etc), tween the triple-point sutures of the nasal, frontal, 49 from the cranium and mandible (foramina, pro- and maxillary bones on each side; Least Interor- cesses, sutures, etc), and 37 from the dentition bital Breadth (LIB), measured at the narrowest point (occlusal morphology, eruption sequences); addi- across the frontals between the orbits, even when tionally we scored four characters representing the postorbital constriction (between the temporal chromosomal fission/fusion events from published fossae) is narrower; Zygomatic Breadth (ZB), karyotypic studies. measured at the widest point across both zygo- We obtained nuclear gene sequences from a matic arches; Palatal Length (PL), measured from single tissue sample of Gracilinanus emiliae the anteriormost point of the premaxillae to the (MUSM 15292), and from tissue samples repre- postpalatine torus, including the postpalatine spine senting all of the other ingroup and outgroup taxa (if present); Palatal Breadth (PB), measured across from which morphological character data were the labial margins of the M4 crowns, at or near the scored, using procedures for DNA extraction, stylar A position; Maxillary Toothrow Length amplification, and sequencing explained by Voss (MTR), measured from the anterior margin of C1 and Jansa (2009). The molecular data analyzed to the posterior margin of M4; Length of Molars herein consist of 7320 aligned base pairs (bp) from (LM), measured from the anteriormost labial mar- five unlinked protein-coding genes: Breast Cancer gin of M1 to the posteriormost point on M4; Length Activating 1 Gene (BRCA1 exon 11; 2163 bp), of M1–M3 (M1–M3), measured from the Dentin Matrix Protein 1 (DMP1 exon 6; 1176 bp), anteriormost labial margin of M1 to the Interphotoreceptor Retinoid Binding Protein (IRBP posteriormost point on M3; Width of M4 (WM4), exon 1; 1158 bp), Recombination Activating 1 measured from the labial margin of the crown at or Gene (RAG1; 2790 bp), and von Willebrand Fac- near the stylar A position to the lingual apex of the tor (vWF exon 28; 963 bp). However, we did not protocone. analyze RAG1 third codon positions (which are Following Voss et al. (2001), a specimen was afflicted by severe base-compositional heterogene- judged to be juvenile if dP3 is still in place; sub- ity; Gruber et al., 2007), nor did we analyze DMP1 adult if dP3 has been shed but P3 is still incom- sequences from nondidelphid outgroups (which pletely erupted; and adult if the permanent denti- cannot be unambiguously aligned with opossum tion is complete. Qualitative character variation is sequences; Jansa et al., 2006). described herein using terminology that is explained We analyzed these data (morphological, karyo- or referenced by Voss and Jansa (2003, 2009). An typic, and molecular) simultaneously using maxi- exception (not defined by those authors) is the mum parsimony (MP) as implemented by PAUP* prefix “self-” as used in combination with descrip- ver. 4.0b10 (Swofford, 1998). All molecular char- tors of ventral pelage color, such as self-white or acters were treated as unordered and equally self-cream (Tate, 1933). This usage applies to hairs weighted, and the heuristic tree search employed that have the same coloration from base to tip, as 5000 replicates of random stepwise taxon addition 436 Mastozoología Neotropical, 16(2):433-443, Mendoza, 2009 RS Voss et al. http://www.sarem.org.ar followed by tree bisection-reconnection (TBR) branch swapping. We assessed nodal support us- ing nonparametric bootstrapping (Felsenstein, 1985) as implemented by PAUP* (from 1000 pseudoreplicated datasets, each heuristically ana- lyzed with 10 random-addition replicates and TBR branch swapping), and by computing Bremer sup- sometimes port values (Bremer, 1994) as implemented by TreeRot (Sorenson, 1996).

RESULTS

Diagnostic characters and phenotypic weakly beaded

variability gray-based buffy gray-based buffy

Gracilinanus emiliae can be unambiguously distinguished from other congeneric species by a unique combination of morphometric and erior absent absent iliae marica microtarsus

qualitative characters (Table 1). Externally, G. beaded self-white cusp present

emiliae is distinctively long-tailed, with a ra- reddish-brown reddish-brown reddish-brown tio of tail to head-and-body length that aver- ages 1.80, much larger than any value we have computed from other congeners. Additionally, G. emiliae is the only currently recognized species of Gracilinanus with self-white under- dryas em parts, all other species having gray-based buffy absent post dark brown or brownish ventral fur. Mature adult speci- mens of G. emiliae have distinctly beaded Table 1 supraorbital margins but no postorbital pro- cesses (Fig. 1). Whereas other congeners have large and distinct maxillary vacuities, these palatal openings are very small or absent in agilis G. emiliae. The unworn upper canine (C1) of G. emiliae has a posterior accessory cusp that usually absent is absent in other species of Gracilinanus, and the molars of G. emiliae are distinctively small. species. Tabulated traits are those of adult specimens (juveniles and subadults may not exhibit all features). External and craniodental measurements of adult and subadult specimens of Gracilinanus orange gray-based buffy gray-based brownish beads or no beads or no beads or (N = 5) (N = 22) (N = 10) (N = 5) (N = 7) (N = 7) emiliae exhibit remarkably little intraspecific (N = 3) (N = 6) (N = 6) (N = 4) (N = 5) (N = 3) 1–5.6 mm 5.6–5.9 mm 5.4–5.8 mm 4.8–5.1 mm 5.3–5.6 mm 5.7–6.0 mm processes processes processes with processes aceramarcae reddish-brown reddish-brown variation (Table 2). Close scrutiny of these well-developed well-developed well-developed small or absent well-developed well-developed Gracilinanus specimens, including side-by-side comparisons of skulls from the Guianas, Colombia, Brazil, and Peru did not reveal any conspicuous mor- phological differences among them that could not be attributed to age or individual varia- s: absent

tion. In short, there seems to be no compelling cusp phenotypic evidence that more than a single species is represented in the material at hand. However, given the broad distribution of this Upper molar length (LM): 5. Adult LT/HBL ratios:Dorsal pelage: 1.50–1.52 1.34–1.45 1.20–1.68 1.64–1.96 1.32–1.38 1.25–1.38 Maxillary fenestrae: C1 accessory taxon, it is possible that two or more morpho- pelage:Ventral Interorbital region: gray-based no Selected diagnostic characters of SYSTEMATICS OF Gracilinanus emiliae 437

logically cryptic but genetically distinct forms are present. At the moment, we are unable to evaluate this possibility.

Ecogeographic distribution Eight localities from which we have exam- ined specimens that exhibit the diagnostic characteristics of Gracilinanus emiliae as de- scribed above are mapped in Fig. 2. Most other localities from which G. emiliae has previ- ously been reported by authors are based on misidentified or lost specimens. Although Voss et al. (2001: 29-30) provided correct identifi- cations for some of these and emphasized the dubious validity of others, their results were ignored by Brown (2004: fig. 20), whose dis- tribution map for G. emiliae included five erroneous or dubious records. Among the in- valid records mapped by Brown are two Bra- zilian localities originally reported by Patterson (1992) based on juvenile specimens of Fig. 1. Dorsal, ventral, and lateral views of the skull Marmosa lepida (see Voss et al., 2001: 29- and mandible of Gracilinanus emiliae. This 30). A third invalid record is the type locality drawing (modified from Voss et al., 2001: figs. 11, 12) is a composite based on several speci- of “Marmosa” agricolai, Moojen, 1943, a mens, none of which is anatomically complete taxon that Gardner and Creighton (1989) con- (AMNH 203363, 267006; ROM 35466). sidered a junior synonym of G. emiliae but

Table 2 Provenance, age, sex, measurements (mm) and weights (g) of subadult and adult specimens of Gracilinanus emiliae. Notes: a Type of Marmosa emiliae Thomas. b Type of Gracilinanus longicaudus Hershkovitz. c Remeasured from fluid specimen. d Estimated value. e Tate’s (1933: table 1) value of 5.3 mm for the interorbital breadth of this specimen (repeated in Hershkovitz, 1992: table 5) is erroneous. f Value from Hershkovitz (1992: table 5); the right zygomatic arch of this specimen is now broken.

BMNH AMNH AMNH ROM FMNH MUSM 9.3.9.10a 203363 267006 35465 87924b 15292 Country of origin Brazil Brazil French Guiana Guyana Colombia Peru Age subadult adult subadult adult adult adult Sex male male male female male female HBL 75 80 75 83 87 77 LT 142 150 138 142 143 151 HF 13 14 13c 14 16 16 Ear 16 15 17 17 16 17 CBL 22.0 23.7 21.3 23.8 23.8 23.2 LM 4.9d 5.0 4.9 d 5.1 5.0 4.8 M1–M3 4.2 4.4 4.1 4.4 4.4 4.2 PB 7.0 — — 7.5 7.7 6.9 PL 11.9 12.9 11.7 12.8 12.9 12.6 LIB 4.2e — 3.9 4.2 4.2 4.2e ZB 12.8 — 12.7 14.0 13.4f 14.0 Weight — 10 10 — — 14 438 Mastozoología Neotropical, 16(2):433-443, Mendoza, 2009 RS Voss et al. http://www.sarem.org.ar

Fig. 2. Geographic distribution of collection localities based on specimens examined by the authors (•) and others reported in the literature (). Specimens that we examined are from: 1. Brazil, Pará, “Para” (= Belém, type locality; 1º27’S, 48º29’W, 10 m); 2. Brazil, Pará, Capim (1º41’S, 47º47’W, 25 m); 3. Colombia, Meta, Los Micos (3º17’N, 73º53’W, 450 m); 4. French Guiana, Paracou (5º17’N, 52º55’W, 25 m); 5. Guyana, Upper Takutu-Upper Essequibo, 12 km E Dadanawa (ca. 2º50’N, 59º31’W, ca. 150 m); 6. Peru, Loreto, Nuevo San Juan (5º15’S, 73º10’W, 150 m); 7. Surinam, Marowijne, Langamankondre (5º43’N, 54º01’W, sea level); and 8. Venezuela, Monagas, Hato Mata de Bejuco (ca. 9º19’N, 62º56’W, 18 m). Localities reported by Linares (1997, 1998) based on specimens that we have not seen are: A. Venezuela, Bolívar, San Ignacio de Yuruaní (5º01’N, 61º09’W, 850 m); and B. Venezuela, Falcón, 19 km NW Urama (10º34’N, 68º21’W, 25 m).

which exhibits many inconsistent morphologi- specimen was recently reidentified by Astúa cal characters (Voss et al., 2001: 29). Recently, (2006) as Hyladelphys kalinowskii. Voss et al. (2005) referred agricolai to the A fifth locality for Gracilinanus emiliae genus Cryptonanus. mapped by Brown (2004) that is almost cer- Another erroneous locality for Gracilinanus tainly erroneous is Santarem. This record is emiliae mapped by Brown (2004) was origi- based on a specimen in the British Museum nally reported by Ávila-Pires (1964). Although that Thomas (1888: 349) identified as Ávila-Pires did not provide a museum catalog “Didelphys pusilla” and that Tate (1933) iden- number for the specimen in question and did tified as “Marmosa microtarsus”. Neither not say where it came from or who collected Thomas nor Tate provided a catalog number, it, the only possible match appears to be MNRJ but handwritten annotations in Thomas’s per- 20918 (originally INPA 1045), which was sonal copy of his 1888 monograph indicate collected at or near Manaus by M.C. Mello in that it was BMNH 54.11.14.3, corresponding 1957 (J.A. de Oliveira, pers. comm.). This to material originally purchased from SYSTEMATICS OF Gracilinanus emiliae 439

Stevens—a commercial dealer in natural his- tory specimens—and apparently now lost (P. Jenkins, pers. comm.). It is not clear why Hershkovitz (1992) identified this specimen as emiliae sight unseen, given that Tate (1933) had not done so when he saw it in London with the holotype of emiliae at hand. We are currently unable to evaluate two Venezuelan records of Gracilinanus emiliae reported by Linares (1997, 1998). Although his morphometric data are largely consistent with that identification (we assume that his measurement “m2–4” corresponds to m2–5 of Fig. 3. Phylogenetic relationships among thylamyine based on a heuristic parsimony analy- Hershkovitz [1992], which is equivalent to LM sis of morphological characters and DNA se- of the present study), some diagnostic traits quences. Bootstrap percentages are provided were omitted from his description, and no above each branch, decay (Bremer) support specimen numbers were provided. Only one below. “Other didelphids” include 27 species belonging to the subfamilies , of his records falls slightly outside the known Glironiinae, Hyladelphinae, and Didelphinae geographic range of G. emiliae as documented (tribes Marmosini, Metachirini, and by specimens that we have personally exam- Didelphini); “outgroups” include seven species ined. of nondidelphid marsupials (caenolestids, Dromiciops, dasyurids, and peramelids). Our new material, which represents a range extension of about 950 km, consists of a single adult female specimen (MUSM 15292) col- lected on 7 September 1999 near Nuevo San genera comprising the tribe Thylamyini. Al- Juan, a Matses Indian village on the Río though Gracilinanus and Cryptonanus were Gálvez, a left-bank tributary of the Río Yavarí, consistently recovered as sister taxa, support in the Peruvian department of Loreto (Fig. 2: for this relationship is weak. locality 6). This was shot at night by a Whereas previous analyses of nonmolecular Matses hunter who saw it perched on a branch (morphological + karyotypic) and molecular of a small tree in the subcanopy of well-drained characters yielded conflicting and weakly sup- primary lowland rain forest. No savannas or ported hypotheses about the relationships of other natural nonforest vegetation is present Gracilinanus emiliae to other thylamyines in the ca. 8000 km2 drainage basin of the Río (Voss et al., 2005; Jansa and Voss, 2005; Jansa Gálvez nor in any of the other adjacent low- et al., 2006), the phylogenetic position of G. land watersheds between the Río Ucayali and emiliae is now convincingly resolved as the the Río Yavarí. sister taxon of all other Gracilinanus species in our analysis. Although G. dryas, G. marica, Phylogenetic relationships and at least one undescribed species remain to The strict consensus of 12 equally most- be analyzed phylogenetically, their morpho- parsimonious trees recovered by our combined logical attributes suggest that they are more analysis of morpholological, karyotypic, and closely related to G. agilis, G. microtarsus, molecular data is almost completely resolved, and G. aceramarcae than they are to G. and most suprageneric nodes are strongly sup- emiliae. ported (Fig. 3). As in Bayesian and likelihood analyses of these data (Voss and Jansa, 2009), DISCUSSION Gracilinanus was found to be deeply embed- The new Peruvian specimen provides incon- ded within a monophyletic cluster of didelphine trovertible evidence that Gracilinanus emiliae 440 Mastozoología Neotropical, 16(2):433-443, Mendoza, 2009 RS Voss et al. http://www.sarem.org.ar occurs in primary lowland rain forest. Several intensive multi-year faunal inventory efforts other examined specimens might also have have been carried out (e.g., Paracou, French been collected in this habitat (Table 3), but Guiana; Voss et al., 2001). Apparently arbo- only two are accompanied by definite infor- real, it is unlikely to be captured unless a mation about the vegetation in which they were special effort is made to thoroughly sample taken. One of these (from Paracou, French the arboreal fauna, but weighing only 10 to Guiana; locality 4) was shot at night from a 14 g (Table 2) it is probably too small to be tree where it perched about 4 m above the taken in most commercially manufactured traps ground in dense secondary growth next to a (e.g., those used by Malcolm, 1991). Addi- road through primary lowland rain forest, and tionally, like other small didelphids, it may be the other (from 47 km E Maturín, Venezuela; unattracted to most commonly used baits. locality 8) was trapped on a vine in lowland Therefore, the absence of any specimens from gallery forest. Lowland rain forest is the domi- central Amazonia may simply be an artifact of nant vegetation formation in northeastern Pará inadequate or inappropriate collecting efforts. (localities 1 and 2), and this habitat is present Given the geographic dispersion of collect- as riparian growth in the Rupununi savannas ing localities (Fig. 2) and the difficulty of around Dadanawa (locality 5). Los Micos, collecting specimens even where the species Colombia (locality 3) is on the rainforested is known to occur, it seems probable that eastern flanks of the Serranía de la Macarena Gracilinanus emiliae occurs throughout the near the western margin of the Llanos. Amazonian lowlands and (if Linares’ [1997, Langamankondre (locality 7) is on the west 1998] specimens were correctly identified) it bank of the Marowijne River, in a part of may also be widespread in Venezuelan coastal Surinam where gallery forests commonly in- rainforests (sensu Voss and Emmons, 1996). terrupt the coastal savannas. The most plau- If true, this would explain an otherwise puz- sible interpretation of these data is that zling gap in the distribution of the genus, Gracilinanus emiliae is a lowland rainforest various species of which inhabit almost every species that occurs in both primary and sec- other forested region of tropical and subtropi- ondary formations and in gallery forests within cal South America (Table 4). No matter what some savanna-dominated landscapes. phylogenetic hypothesis is supported when G. Gracilinanus emiliae is obviously hard to dryas, G. marica, and at least one undescribed collect. No more than a single specimen is species are included in future analyses, the known from any locality, even those where biogeographic history of the genus has obvi-

Table 3 Ecological data associated with examined specimens of Gracilinanus emiliae. Numbered localities refer to those mapped in Fig. 2.

Locality Habitat

1. Brazil, Belém Unknown (probably lowland rain forest) 2. Brazil, Capim Unknown (probably lowland rain forest) 3. Colombia, Los Micos Unknown (probably lowland rain forest but savannas nearby) 4. French Guiana, Paracou Roadside secondary growth next to primary lowland rainforest, but savannas nearby (Voss et al., 2001) 5. Guyana, 12 km E Dadanawa Unknown (local vegetation includes savanna and evergreen gallery forest; Robbins et al., 2004) 6. Peru, Nuevo San Juan Primary lowland rain forest (this report) 7. Surinam, Langamankondre Unknown (possibly lowland rain forest but savannas nearby) 8. Venezuela, Hato Mata de Bejuco Gallery forest (Linares, 1997) SYSTEMATICS OF Gracilinanus emiliae 441

Table 4 Ecogeographic distribution of Gracilinanus species. Notes: a See Voss et al. (2004: table 12). b See Costa et al. (2003). The taxonomic status of peruanus Thomas, 1931, remains to be convincingly established, but if it is a synonym of agilis Burmeister, 1854, then the range of the latter would extend into the premontane and lowland rainforests of SE Peru. We believe that the Venezuelan material identified as G. agilis by Linares (1997, 1998) is misidentified. c See Handley (1976) and Linares (1998). d This report. e See Handley (1976), Linares (1998), and Creighton and Gardner (2008). The unpublished Trinidadian record is based on AMNH 206763 from Bush Bush Forest (10º24’N, 61º03’W, near sea level; Downs et al., 1968). f See Costa et al. (2003). g Represented by three examined Colombian specimens, one from Unguía in Departamento Chocó (FMNH 69849), another from Turbaco in Departamento Bolívar (USNM 399950), and a third from San José in Departamento Valle de Cauca (AMNH 31693).

Species Distribution

G. aceramarcae Montane rain forests between 2530 and 3350 m in the Andes of N Bolivia and S Perua G. agilis Moist and dry forests of central Brazil, E Paraguay, NE Argentina, and E Boliviab G. dryas Montane rain forests between 2200 and 4000 m in the Andes of W Venezuela and NE Colombiac G. emiliae Lowland rain forests and gallery forest, probably throughout Amazonia and N Venezuelad G. marica Premontane and montane rainforests between 720 and 2590 m in the Serranía de Perijá of N Colombia and in the Andes and coastal sierras of Venezuela; also near sea level in Trinidade G. microtarsus Lowland and premontane rain forests of SE Brazilf G. sp. nov. TransAndean lowland rainforest in Colombia and probably E Panamag

ously covered most of the continental land- rior accessory cusps in Cryptonanus (see Voss scape at low latitudes. How the Amazonian et al., 2005: fig. 3A); most species of distribution of G. emiliae fits into this puzzle Gracilinanus lack accessory canine cusps remains to be determined. (Voss et al., 2005: fig. 3B), but a posterior The recovered position of Gracilinanus accessory cusp is present on C1 in G. emiliae. emiliae as phylogenetically intermediate be- Although the relationships we recovered tween Cryptonanus on the one hand and the within Gracilinanus could be recognized in- clade formed by G. aceramarcae + G. agilis formally (as the basis for “species groups”) or + G. microtarsus on the other is not altogether formally (by naming subgenera), such actions unexpected given the morphological distinct- seem premature given our still-incomplete ness of emiliae from other congeneric species. taxon sampling and the likelihood that more Indeed, G. emiliae could be interpreted as species remain to be discovered or resurrected morphologically transitional in some charac- from synonymy. Plausibly, such discoveries ters. For example, whereas maxillary fenes- may come from closer morphological study of trae (maxillary perforations that lie between available specimens, from sequence data rep- the maxillopalatine fenestra and M1 on either resenting hitherto unsampled nominal taxa side of the palate; Voss and Jansa, 2003: fig. (e.g., peruana Tate, 1931), and from new 5) are absent in Cryptonanus and well devel- collecting efforts in landscapes where the ge- oped in most species of Gracilinanus, they nus is still unknown (e.g., most of the north- are always small and occasionally absent (uni- ern and central Andes). Future analyses based laterally or bilaterally) in G. emiliae. Another on additional characters and more comprehen- example is the morphology of C1, which is sive taxon sampling will doubtless provide a more often provided with both anterior and poste- secure basis for intrageneric classification. 442 Mastozoología Neotropical, 16(2):433-443, Mendoza, 2009 RS Voss et al. http://www.sarem.org.ar

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